The Sensitivity of Children to Electromagnetic Fields
Leeka Kheifets, Michael Repacholi, Rick Saunders and Emilie van Deventer
Pediatrics 2005;116;303-313
DOI: 10.1542/peds.2004-2541
This information is current as of May 17, 2006
The online version of this article, along with updated information and services, is
located on the World Wide Web at:
http://www.pediatrics.org/cgi/content/full/116/2/e303
PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly
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SPECIAL ARTICLE
The Sensitivity of Children to Electromagnetic Fields
Leeka Kheifets, PhD*; Michael Repacholi, PhD‡; Rick Saunders, PhD‡; and Emilie van Deventer, PhD‡
ABSTRACT. In today’s world, technologic developments bring social and economic benefits to large sections of society; however, the health consequences of
these developments can be difficult to predict and manage. With rapid advances in electromagnetic field (EMF)
technologies and communications, children are increasingly exposed to EMFs at earlier and earlier ages. Consistent epidemiologic evidence of an association between
childhood leukemia and exposure to extremely low frequency (ELF) magnetic fields has led to their classification by the International Agency for Research on Cancer
as a “possible human carcinogen.” Concerns about the
potential vulnerability of children to radio frequency
(RF) fields have been raised because of the potentially
greater susceptibility of their developing nervous systems; in addition, their brain tissue is more conductive,
RF penetration is greater relative to head size, and they
will have a longer lifetime of exposure than adults. To
evaluate information relevant to children’s sensitivity to
both ELF and RF EMFs and to identify research needs,
the World Health Organization held an expert workshop
in Istanbul, Turkey, in June 2004. This article is based on
discussions from the workshop and provides background information on the development of the embryo,
fetus, and child, with particular attention to the developing brain; an outline of childhood susceptibility to environmental toxicants and childhood diseases implicated
in EMF studies; and a review of childhood exposure to
EMFs. It also includes an assessment of the potential
susceptibility of children to EMFs and concludes with a
recommendation for additional research and the development of precautionary policies in the face of scientific
uncertainty. Pediatrics 2005;116:e303–e313. URL: www.
pediatrics.org/cgi/doi/10.1542/peds.2004-2541; children,
environmental risk, policies, sensitive periods, mobile
phones, electromagnetic fields, power lines.
ABBREVIATIONS. ELF, extremely low frequency; IARC, International Agency for Research on Cancer; RF, radio frequency; EMF,
electromagnetic field; WHO, World Health Organization; CNS,
central nervous system; ALL, acute lymphoblastic leukemia;
AML, acute myeloblastic leukemia; SAR, specific absorption rate.
From the *Department of Epidemiology, University of California School of
Public Health, Los Angeles, California; and ‡Radiation and Environmental
Health, World Health Organization, Geneva, Switzerland.
Accepted for publication Feb 2, 2005.
doi:10.1542/peds.2004-2541
The opinions in this paper are the sole responsibility of the authors and do
not represent the position of the World Health Organization.
Conflict of interest: Dr Kheifets worked and consulted for Electric Power
Research Institute and Utilities (Palo Alto, CA), and Dr Saunders worked
for the National Radiation Protection Board (Oxfordshire, United Kingdom).
Address correspondence to Leeka Kheifets, PhD, Department of Epidemiology, UCLA School of Public Health, 73-284 CHS, 50 Charles E. Young Dr
S, Los Angeles, CA 90095-1772. E-mail: [email protected]
PEDIATRICS (ISSN 0031 4005). Copyright © 2005 by the American Academy of Pediatrics.
C
hildren in both industrialized and developing
countries are exposed to a large variety of
environmental agents including indoor and
outdoor air pollution, water and food contaminants,
chemicals (eg, pesticides, lead, mercury), and physical agents such as ultraviolet radiation and excessive
noise. Changes in exposure to these agents are being
linked to real or perceived increases in the incidence
of certain childhood diseases, such as asthma, leukemia, and brain cancer, and in some behavioral and
learning disabilities. Environmental exposures can
be particularly harmful to children because of their
special vulnerability during periods of development
before and after birth.
Exposure to electric and magnetic fields from 0 to
300 GHz has been increasing greatly as countries
increase their capacity to generate and distribute
electricity and take advantage of the many new technologies, such as telecommunications, to improve
lifestyle and work efficiency (Fig 1). Evidence of an
association between childhood leukemia and exposure to extremely low frequency (ELF) magnetic
fields has led to their classification by the International Agency for Research on Cancer (IARC) as a
“possible human carcinogen”1 based on consistent
epidemiologic data and lack of support by laboratory
studies in animals and cells. The reason why the
results of the childhood leukemia studies are consistent is still being investigated, but one possibility is
that children may be more sensitive to radiation in
some or all parts of the electromagnetic spectrum.
Concerns about the potential vulnerability of children to radio frequency (RF) fields from mobile telephony were first raised by an expert group in the
United Kingdom2 on the grounds that children have
a longer lifetime of exposure than adults, and from a
physiologic point of view, they have a developing
nervous system, their brain tissue is more conductive
than that of adults because it has a higher water
content and ion concentration, and they have greater
absorption of RF energy in the tissues of the head at
mobile telephone frequencies. This topic was discussed further at a European Cooperation in the
Field of Scientific and Technical Research (COST) 281
workshop,3 in a report of the Health Council of the
Netherlands,4 and in a recent report from the United
Kingdom’s National Radiological Protection Board.5
To evaluate the available information relevant to
children’s sensitivity to electromagnetic fields
(EMFs) and to identify research needs, the World
Health Organization (WHO) held an expert workshop in Istanbul, Turkey, in June 2004. This article is
based on discussions and recommendations from the
workshop and provides background information on
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e303
Fig 1. Electromagnetic spectrum. VDUs indicates video display units.
the development of the embryo, fetus, and child,
with particular attention to the developing brain; an
outline of childhood susceptibility to environmental
toxicants, childhood diseases implicated in EMF
studies, and exposure to ELF and RF fields, with a
focus on children. After a brief presentation of the
EMF science most pertinent to effects on children
and a review of several proposed mechanisms, the
potential sensitivity of children to EMFs is discussed.
Finally, recommendations are outlined on the protection of children through the development of precautionary approaches in the face of scientific uncertainty.
FROM EMBRYO TO ADOLESCENCE
Embryo, Fetal, and Childhood Development
Development proceeds from conception to adulthood through a number of different stages in which
the developmental processes are markedly different,
and their susceptibility to environmental teratogens
varies. The prenatal period of development is divided roughly into 3 periods: the preimplantation
period, extending from fertilization to the settling of
the embryo into the uterine wall; a period of organogenesis, characterized by the formation of the
main body structures; and the fetal period, during
which growth of the structures already formed takes
place. Additional developmental changes take place
after birth. Postnatal changes are characterized by
slower growth and maturation of existing organ systems, notably the central nervous system (CNS), the
hemopoietic and immune systems, the endocrine
and reproductive systems, and the skeletal system.
The completion of sexual development at the end of
the second or the beginning of the third decade of
human life marks the completion of this period of
growth and maturation. Essentially, however, the
nature of the toxicant and the timing and magnitude
of exposure determine the risk of any adverse effects
in terms of both severity and occurrence. Vulnerabile304
ity can vary quite rapidly during the prenatal period,
whereas slower changes occur postnatally.6
During the first 2 weeks of embryonic development (known as the “all-or-none period”), the embryo is very sensitive to the lethal effects of toxic
agents and much less sensitive to the induction of
malformation. Many of the cells are still omnipotential stem cells, and if the embryo survives a toxic
exposure it can recuperate without an increased risk
of birth defects or growth retardation. During the
next 6 to 8 weeks of development, major organogenic
events occur and toxic agents with teratogenic potential can cause major malformations of the visceral
organs, the CNS, the face, and the limbs. From the
8th to the 15th week, neuron proliferation, differentiation, and migration in the CNS are particularly
vulnerable.7 Genitourinary and other malformations,
gonad cell depletion, and neurodevelopmental problems may occur if the thresholds for these effects are
exceeded. During the late fetal period, effects on
growth of the fetus and susceptible organs such as
the CNS diminish, but vulnerability to deleterious
effects remains high compared with adults.
Development continues after birth, but now this
process largely entails the maturation of existing organ systems, although growth is still occurring. Neurobiologists long believed that neurogenesis in the
human ends during the first months of postnatal life,
but recent rodent and primate studies demonstrate
that there is lifelong neuron production in some
parts of the CNS.8 However, with some particular
exceptions, most adult neurons are already produced
by birth. The number of connections (synapses) between neurons in the human brain peaks at ⬃2 years
and decreases by 40% to the adult number during
adolescence8 as experience is acquired and “redundant” connections lost. This reflects the balance between the formation of new synapses (synaptogenesis) and synapse elimination, a “pruning” back of
excess synapses between neurons, which are key
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processes in the development of the postnatal “hardwiring” of the brain. Another important neurologic
event that occurs postnatally is myelination, which
facilitates the transmission of information within the
CNS and occurs most rapidly from birth to 24
months but may also continue into the second decade. Unfortunately, the susceptibility of these processes to environmental agents has not been studied
extensively and thus is not well understood. However, because developmental processes are vulnerable to disruption by agents that may not be toxic to
mature systems, it is reasonable to expect that the
later stages of brain development present special
risks.8
Other threshold effects that can result from postnatal exposures include interference with fertility
and endocrine function, alterations in sexual maturation, and interference with the development of the
immune system. Endocrine disrupters, exogenous
substances that mimic the action of hormones (particularly steroids), may alter the function of the developing endocrine system and have adverse effects
on the reproductive organs, liver, kidney, adrenal
glands, CNS, immune system, cardiovascular system, and bones.9
Exposure to toxic agents with mutagenic and carcinogenic potential, such as ionizing radiation, cancer chemotherapeutic drugs, and some chemicals,
poses theoretical, stochastic risks for the induction or
progression of cancer during embryonic and childhood development. However, although many agents
have been alleged to be responsible for cancer and
genetic disease, such effects will only result from
agents that have either mutagenic properties or the
ability to produce more subtle effects on carcinogenic
processes, such as the stimulation of excessive cell
proliferation or an influence on cell-to-cell communication, apoptosis, or DNA repair.
males exposed in utero developed masculine behaviors, and males showed exaggerated male mating
behaviors. These observations suggest that these
chemicals masculinized by mimicking steroid hormones or by changing hormone levels.
Of perhaps more specific interest are toxic exposures that affect the nervous system of the fetus,
infant, and child. Because development of the nervous system is very specific in pattern and timing,
exposure to various agents at critical periods of development can cause long-lasting or permanent injury. For instance, exposure to ethanol or methylmercury has been shown to affect neuronal proliferation
in rodents and in other experimental models. Some
agents such as ethanol, lead, methylmercury, and
some pesticides seem to affect synaptogenesis. Each
of the multiple processes of neural development has
been shown to be affected by specific toxic agents,
often at low doses but at critical periods of development.
The timing of exposure might be critical as well:
for ionizing radiation, excess risk for leukemias and
brain and thyroid cancer is higher for exposures that
occur in childhood; the risk of breast cancer was
highest for Japanese women exposed to ionizing radiation from the atomic bomb during puberty, although the risk also increased in women who were
⬍10 years old (an age at which girls have little or no
breast tissue) at the time of the explosion.11 Similarly,
sunburns in childhood seem to be particularly potent
in increasing the risk of skin cancer later in life.12
Exposure in childhood may also increase the risk of
disease later in life simply because the duration of
exposure can be much longer if it starts early. There
is evidence, for instance, that the younger a person is
when starting smoking, the higher the risk of lung
cancer.13
Children’s Susceptibility to Environmental Exposures
Some diseases are limited to the embryo, child, or
adolescent; other diseases that occur in children and
adults manifest themselves differently in children.
Of particular relevance to EMF exposure are childhood leukemia and brain cancer. There is consistent
evidence from epidemiologic studies of a risk of
childhood leukemia associated with exposure to environmentally high levels of ELF magnetic fields.
There is no explanation for this effect from laboratory studies. An increased risk of brain cancer has
been investigated in relation to ELF exposures and
has been raised particularly in the context of mobilephone use and the absorption of RF signals by the
brain, although there is no convincing evidence suggesting an increased risk. To put potential EMF effects in perspective and determine how EMFs might
be involved in the development of these diseases, we
provide a brief overview of rates and risk factors for
them.
Several aspects of exposure and susceptibility warrant a focus on children. In some exposure scenarios,
children may receive higher doses than adults, resulting from higher intake and accumulation or differences in behavior. Greater susceptibility to some
toxicants and physical agents has been demonstrated
in children. Because the period from embryonic life
to adolescence is characterized by growth and development, deleterious effects can occur at lower levels
and be more severe or lead to effects that do not
occur in adults; on the other hand, children can be
more resilient because of better recuperative capacities.
Toxic exposures in utero have produced effects
that are quite surprising, given the period or level of
exposure. Cassidy et al10 reported that exposure to
the persistent organochlorine chlordane in utero at
quite low levels causes significant long-term alterations in sexual behavior. These effects were evident
at levels of exposure very similar to those experienced in homes in the United States when chlordane
and heptachlor were universally applied as termiticides. Both of these chemicals produced marked
changes in sexually dimorphic functions in rats; fe-
Childhood Diseases Relevant to EMF Exposure
Childhood Leukemia
Leukemias are the most common cancer to affect
children, accounting for 25% to 35% of all childhood
malignancies. The biological heterogeneity of childhood leukemia is well documented; the major mor-
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phologic types are acute lymphoblastic leukemia
(ALL) and acute myeloblastic leukemia (AML).
The rate of leukemia for children ⬍15 years old has
been estimated to be ⬃4 per 100 000 per year in the
developed world and 2.5 per 100 000 per year in the
developing world.14 In developed countries, the incidence of leukemia rises rapidly after birth, peaking
at ⬃3 years of age before declining and then rising
steadily again throughout life. Thus, unlike many
cancers, it has a short latency and a peak incidence
early in life15 that has resulted in many etiologic
hypotheses, most notably those involving exposure
to infections.16
Subtypes of AML and ALL are frequently characterized by genetic alterations, including changes in
chromosome number (hyperdiploidy or hypodiploidy) and chromosomal translocations that may involve chimeric or fusion genes.17,18 These genes include MLL, TEL, and AML1, all of which can fuse
with many other genes and, in the case of TEL and
AML1, with each other. There is strong evidence that
this rearrangement may originate in utero, supported by data obtained from studies of identical
twins or children with concordant ALL. Screening of
newborn blood samples suggests that ⬃1% have the
TEL-AML1 gene fusion, 100 times the proportion of
children that will develop ALL with a TEL-AML1
gene fusion before the age of 15 years. This implies
that the conversion of the preleukemic clone to overt
disease is low and that development of childhood
ALL is a multistep process requiring at least 1 prenatal event in combination with additional prenatal
and/or postnatal events. Although the “first hit,” the
initiating in utero event, is believed to be common,
the “second hit,” possibly occurring postnatally, is
rare and therefore acts as the rate-determining step
in development of the disease.
As with most other cancers, the mechanism by
which leukemia arises is likely to involve gene-environment interactions, the environmental exposures
being derived from both endogenous and exogenous
sources. Accordingly, it is important to identify exposures that either cause DNA damage and induce
chromosome breaks that are repaired inadequately
or act as promoters and/or progressers, ultimately
leading to the overt expression of the disease. Exposures acting before birth and early in life have long
been thought to be important determinants of leukemia; it is unfortunate that the evidence regarding the
majority of suggested exposures is limited and often
contradictory. Ionizing radiation given at large doses
is one of the few known risk factors for leukemia.
Brain Cancer
CNS tumors account for ⬃20% of all malignancies
in children ⬍15 years old19 but account for ⬍2% of
cancers in adults. CNS cancers in children occur in
tissues of mesodermal or embryonic origin, but in
adults they occur in epithelial tissues. Another difference between childhood and adult tumors is that
adult tumors tend to occur in the cerebral hemispheres, whereas the majority of pediatric tumors are
brainstem gliomas.
The international incidence rates of childhood
e306
CNS tumors (0 –14 years) vary between developed
and developing nations, with the higher rates observed in most Westernized countries reaching 3 per
100 000 per year compared with 1 to 2 per 100 000 in
other parts of the world.19 Over recent decades,
steady rises in the incidence of childhood CNS tumors have been observed in several populations of
the United Kingdom, the United States, Japan, and
Australia. The debate continues over whether these
increases are “real” or an artifact of improved diagnostic practice and case finding by cancer registries.
The causes of CNS cancers are largely unknown,
although up to 5% may be explained by genetic
predisposition, associated with disorders such as
neurofibromatosis type I.20,21 Having a parent or sibling with a CNS tumor also increases the risk. The
identification of environmental risk factors for CNS
tumors has generally been inconsistent.20,21 Again,
ionizing radiation given in therapeutic doses is one
of the few known risk factors for CNS tumors.
CHILDRENⴕS EXPOSURE TO RF AND ELF FIELDS
In evaluating the potential role of environmental
exposures in the development of childhood diseases,
it is important to consider not only the fact that
childhood exposures can be different from exposures
during adulthood but also the fact that they can be
highly age dependent. Exposures of interest during
the preconception and gestation periods include residential and parental exposures to ELF and RF fields,
including mothers’ exposure from use of domestic
appliances and mobile phones. Infants and toddlers
are exposed mostly at home or at day care facilities.
Among preteens, exposure sources expand to include mobile-phone use and sources at school, with
an increased use of mobile phones in adolescence.
Here we focus on 2 major exposure scenarios: residential ELF and RF exposures and exposure from
mobile phones.
Residential Exposure
Everyone is exposed to ELF electric and magnetic
fields at home.22 High-voltage power lines are a major source of exposure for children who live near
them; however, only ⬃ 1% of children live in close
proximity to high-voltage lines. For most children,
exposure to low-level fields from primary and secondary distribution wiring is continuous; short-duration and intermittent exposure to higher fields results from proximity to domestic appliances. ELF
exposure also occurs at school, during transport, and
even during mobile-phone use. Typical average
magnetic fields in homes seem to be ⬃0.05 to 0.1 ␮T.
Generally, magnetic fields in homes vary from country to country; geometric-mean fields are ⬃35 nT in
the United Kingdom and 70 nT in the United States.
This difference results from the supply voltage used
in the United States (110 V) being approximately half
that used in the United Kingdom (220 V), leading to
approximately twice the electric current and magnetic field exposure. The fraction of homes with average fields above certain thresholds likewise varies;
for example, 1% to 2% of homes in the United Kingdom and 10% in the United States have fields of ⬎0.2
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␮T. Exposure to appliances has been estimated to be
30% of total exposure. Maximum fields experienced
are typically in the tens of microtesla. There is evidence that younger children use appliances less (and
spend less time outside the home), so their personal
exposure is closer to and correlates better with the
fields in the home.
RF fields are produced by radio and television
broadcasts, mobile phones and base stations, and
other communications infrastructure. Radio and television signals are broadcast to a large area from
comparatively few sites. Mobile-phone base stations
cover a smaller area and produce much lower emissions but are now much more common than radio
and television stations (tens of thousands in many
countries). Because of the width and angle of the RF
signal beam and perturbation by the earth and building materials, there is little correlation between field
strength and distance to the source. Typical power
densities outdoors would be 0.01 to 1 mW · m⫺2 but
could be orders of magnitude higher (ie, ⱖ100 mW ·
m⫺2). Depending on where the measurements are
taken, base stations can be the largest individual
source of RF fields, but other sources such as radio or
television transmitters can result in comparable or
greater exposures. Indoor levels are often lower by
orders of magnitude, because buildings screen fields.
A European median indoor power density of 0.005
mW · m⫺2 has been reported.
Background environmental levels are the primary
source of RF exposure for very young children. Potential sources of residential RF exposure to children
are wireless in-house communications (eg, wireless
monitors used in children’s cribs, cordless phones,
Wi-Fi) and mobile-phone use by someone in close
proximity to a child, creating passive exposure. Because children ⬍5 years of age usually spend most of
their time at home, residential exposure can be a
sufficient predictor of individual exposure.22,23 RF
exposure may be estimated more easily for children
than for adults, because the variety of exposure
sources is smaller. When they reach adulthood, today’s children will have a much higher cumulative
exposure to RF fields than today’s adults.
At present, population exposure to RF fields has
been much less characterized than ELF fields, partly
because of technical challenges (lack of adequate
measuring equipment), the rapid evolution of mobile-phone technology (frequency, coding schemes),
and new patterns of use (duration of calls, shortmessage services). However, the main reason ELF
fields are better understood than RF fields is that
they have been studied more.
Mobile-Phone Use
Modern children will experience a longer period of
exposure to RF fields from mobile-phone use than
adults, because they started using mobile phones at
an early age and are likely to continue using them.
Data from a multinational case-control study of potential causes of adult brain cancer show that both
the prevalence of regular mobile-phone users and
daily use are highest in the younger age groups (eg,
19% of younger subjects made calls for ⬎30 minutes
a day, compared with 10% of older subjects).24,25
Moreover, several recent trends (such as increased
popularity, reduced price, and advertising to children) have led to increased mobile-phone use among
children.26 A steep increase in mobile-phone ownership among children has been reported in several
public-opinion surveys.27 For example, in Australia
⬎90% of 6- to 9-year-olds reported sometimes using
their parents’ mobile phones, and in Germany approximately one third of 9- to 10-year-olds reported
owning a mobile phone. Clearly, mobile phones are
the dominant source of RF exposure for teens and
preteens.
HEALTH-RISK ASSESSMENT
The workshop addressed the potential sensitivity
of children at all stages of development from conception through to sexual maturity. The nature of any
adverse health effect that ensues from exposure to an
environmental toxicant depends not only on the timing and magnitude of the exposure but also on the
mechanisms by which the toxicant interacts with the
developing tissue or organ. As a consequence, it is
not possible to generalize about the possible health
effects that might ensue from exposure to an agent
posing unknown risks to health by drawing parallels
with other toxic agents unless they have very similar
mechanisms of interaction. Instead, it is necessary to
examine the experimental and epidemiologic evidence by formulating and testing hypotheses on the
basis of an examination of the known and possible
interaction mechanisms.
Health Risks to Children From ELF Fields
Exposure to ELF EMFs induces electric fields and
currents within the body; guidance on exposure is
based on avoiding the risks to health that result from
the interaction of the induced fields and currents
with electrically excitable nerve tissue, particular that
of the CNS (see, for example, refs 28 and 29). Present
guidance on occupational exposure is based on a
basic restriction on induced current density in the
CNS of 10 mA · m⫺2, which approximates an electric
field in CNS tissue of ⬃100 mV · m⫺1. Guidance on
public exposure incorporates an additional safety
factor, reducing the basic restriction to 2 mA · m⫺2
(20 mV · m⫺1). The basic restrictions are linked to
external field strengths (reference levels) through dosimetric calculation, which is based on realistic anatomic human models and measurements of the dielectric properties of human tissue. For general
public exposure, the corresponding reference levels
for power-frequency electric and magnetic fields are
of the order of 5 kV/m and 100 ␮T, respectively.
Dosimetric calculations have not been conducted
extensively for children and have not been undertaken for pregnant women and their unborn children. In general, adults exposed to ELF electric or
magnetic fields have higher internal electric-field
strengths and current densities than children because
of size and shape differences. However, the distributions are different, and in children some tissues have
higher field strengths and current densities for the
same external field. Furthermore, children have sig-
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nificantly higher internal field strengths and current
densities from contact currents than do adults. Dose
computations using anatomically correct models of
children30 reveal that modest, imperceptible current
into the hand (10 ␮A) produces ⬃50 mV · m⫺1 averaged across the lower-arm marrow of a small child
and approximately ⱖ130 mV · m⫺1 in 5% of that
tissue. During pregnancy, the magnitude and distribution of induced electric fields and currents in the
mother will be different because of changes in body
shape and will not have been assessed in the embryo
or fetus. These factors, along with differences in dielectric properties, need to be taken into account in
assessing health risks to children from ELF EMFs.
The guidance cited above was based on a consideration of laboratory evidence, including evidence
from volunteer studies of magnetic phosphenes, and
more recently on evidence from voltage-gated ion
channel and neural-network behavior.29 Neurobehavioral studies in volunteers and in animals, mostly
in adults, have not reported robust responses to ELF
exposure31; overall, any changes seen have been subtle, transient, and reversible. Workshop participants
thought that there is no reason to suppose a greater
sensitivity of CNS neural networks and ion channels
to induced electric fields in children or in the embryo
or fetus. Reduced myelination seen in childhood and
early adolescence was not thought likely to increase
sensitivity either. It is not clear what the impact
would be of an overabundance of synaptic connections seen in infants and early childhood, but any
increased sensitivity was considered to be covered
by the more restrictive guidance on public exposure.
The evidence that induced electric fields might
affect development of the nervous system and other
tissue was discussed at the workshop in some detail.
Evidence was presented that endogenous direct-current electric fields of 10 to 100 V · m⫺1 played a role
in prenatal development. There is little evidence regarding susceptibility to ELF electric fields, although
it was thought that there is no reason to suppose
greater sensitivity. It was noted that the direct-current electric fields were several orders of magnitude
above present guidance values. However, the possible influence of such fields on synaptogenesis
and/or synapse elimination is not known.
Results from several independent research groups
suggest that exposure to ELF magnetic fields at microtesla levels may disturb early development of
bird embryos. However, replication attempts have
been unsuccessful in some laboratories. Results from
experiments with other nonmammalian experimental models (fish, sea urchins, and insects) have also
suggested subtle effects on developmental stability.32
In mammals, prenatal exposure to ELF magnetic or
electric fields does not result in strong adverse effects
on development. Some effects of magnetic (or combined electric and magnetic) fields on postnatal development have been reported, but evaluation of the
consistency of the findings is difficult because of the
varying methods and approaches used in different
studies.
Numerous epidemiologic studies of various pregnancy outcomes in relation to EMFs are available in
e308
the scientific literature. They include studies investigating the use of video display terminals, electric
blankets, or heated waterbeds, as well as studies of
parental occupational exposure. Most studies have
found no effects, but these studies have been limited
in exposure assessment and lacked the power to
examine high exposure levels. Two studies have included personal measurements of ELF exposure and
reported effects on spontaneous abortion in relation
to maximum measured magnetic fields.33,34 The possibility of exposure assessment bias in these studies
has been discussed, and results need to be confirmed
in additional studies before firm conclusions can be
drawn.
The potential cancer risks to children of exposure
to ELF EMF, estimated from residential proximity to
power sources and from measured fields, have been
investigated in relation to in utero and postnatal time
periods and to paternal exposure. No consistent associations have been observed for childhood CNS
tumors.35 One recent study36 found an increased risk
of childhood leukemia with high maternal occupational exposure during pregnancy.
An increased risk of childhood leukemia has been
found to be consistently associated with exposure to
environmental levels of power-frequency magnetic
fields at levels very much below present guidance.
Initial studies used a surrogate for magnetic fields
(known as wire codes) that was based on distance
and thickness of power lines near the residence.37 As
instruments became available, the focus shifted to
measured or calculated magnetic fields. Results of
dozens of increasingly sophisticated studies and the
2 pooled analyses have reported a doubling of risk
for children exposed to magnetic fields ⬎0.3 to 0.4
␮T compared with children exposed to fields ⬍0.1
␮T.38,39 Although a number of factors, including socioeconomic status, have been evaluated as confounders, substantial confounding has not been identified. However, because of limited knowledge of the
etiology of childhood leukemia, it is difficult to exclude the possibility of some yet-to-be-identified confounder or of confounding by a combination of factors. Nevertheless, substantial confounding of the
observed association, it seems to us, is unlikely. Although these results are also not likely to be a result
of chance, bias cannot be ruled out.40 An epidemiologically detectable risk of leukemia for children, but
not for adults, might result from either better exposure assessment for children or from greater susceptibility in children.
At present there is no experimental evidence that
supports the view that this relationship is causal;
however, few animal studies have been conducted
using animal models of the predominant form of
childhood leukemia, and most carcinogenesis bioassays begin when animals are sexually mature. In
addition, there is no biophysical explanation for biologically significant interactions at these low field
values, so if the association is causal, then there is
currently no scientific explanation. Two hypotheses
for such effects were discussed at the workshop.
One hypothesis discussed at the workshop proposed that the association of power-frequency mag-
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netic fields with childhood leukemia may result from
the flow of electric current through the bone marrow
of children after contact with water fixtures or a
water stream in which a small voltage difference
exists as a result of the grounding of the residential
electrical system to the water pipe.41 Calculation
shows that potentially significant electric fields
(more than ⬃100 mV · m⫺1) may be induced in the
bone marrow in these circumstances; this lends biological plausibility to the proposed mechanism. The
effect of such weak electric fields in inducing effects
in hematopoietic tissue that might increase the risk of
ALL, possibly by affecting preleukemic clones (see
above), has not been investigated.
A second hypothesis suggested that exposure to
power-frequency magnetic fields increases the risk of
childhood leukemia through disruption of the nocturnal production of melatonin in the pineal gland.42
Although the International Commission on Non-ionizing Radiation Protection43 concluded that there is
no convincing evidence of an effect, subtle effects on
melatonin physiology are not easily excluded, and
such studies have not been conducted specifically on
children.
Recommendations were made for additional research regarding the association between exposure
to power-frequency magnetic fields and childhood
leukemia; it is clear that this issue is unresolved.
Although such scientific uncertainty remains, the
WHO recommends the adoption of precautionary
measures for the protection of children (see below).
Health Risks to Children From RF Fields
Exposure to RF radiation induces heating in body
tissues and imposes a heat load on the whole body;
guidance on exposure is based on avoiding the risks
to health that result from localized rises in tissue
temperature and from the physiologic stress engendered by excessive whole-body heat loads.28,29
Present guidance on occupational exposure is based
on restricting the RF-induced whole-body specific
absorption rate (SAR) to ⬍0.4 W · kg⫺1, a heat load
sufficiently small that its contribution to other possible heat loads, generated from hard physical work
and/or imposed by high ambient temperatures, can
be neglected. Basic restrictions on localized SARs,
averaged over any 10 g of contiguous tissue, are 10
W · kg⫺1 in the head and trunk and 20 W · kg⫺1 in the
limbs.28 These are intended to restrict local tissue
temperature rises to acceptable levels. Guidance on
public exposure incorporates an additional safety
factor of 5, reducing the basic restrictions to 0.08 W ·
kg⫺1 to the whole body and 2 W · kg⫺1 to the head.
Temperatures are derived from dosimetric calculation and thermal modeling; SARs are also related to
external field values via dosimetric calculation. The
corresponding reference levels, which for RF fields
are power densities, are frequency dependent and
are of the order of 10 W · m⫺2 at 1800 MHz for
general public exposure.
Dosimetric calculation has for more than a decade
allowed for differences in body size between children and adults, and these differences have been
factored into guidance. Despite large differences in
the size, shape, and tissue distribution of heads, the
SAR values and exposure variations for child models
are similar to those for adults, although somewhat
higher. In addition, the relative depth of penetration
is larger for children, a logical consequence of
smaller head diameter. Dielectric studies encompassing several tissue types, including brain, obtained
from newborn to fully grown rats, mice, and rabbits
exposed to RF EMF in the frequency ranges of 130
MHz to 10 GHz and 300 kHz to 300 MHz report
large, age-related variations in the permittivity and
conductivity of brain tissue and even larger variations for skin and skull tissue.44–46 Thus, there is a
need for dosimetric modeling of the distribution of
SAR and temperature in children and also a requirement for appropriate age-related values for the dielectric properties of tissue.
In addition, the distribution of SAR and temperature should be addressed in pregnancy, taking into
account the fact that the circulation of blood in the
fetus is separate from maternal blood flow. The heat
produced by fetal metabolism is dissipated to the
mother mostly at the placenta, but this is less efficient
than expected and the temperature of the fetus is
usually ⬃0.5°C above that of the mother.47
The difference between the ability of children and
that of adults to dissipate whole-body heat loads is
small. During exercise in thermally neutral or warm
environments, children thermoregulate as effectively
as adults. When ambient temperatures exceed body
temperature, however, children are more liable to
have a higher rate of heat absorption compared with
adults. Also, although neither children nor adults
replace fluid loss sufficiently during exercise in the
heat, dehydration may have a more detrimental effect on children because of their greater reliance on
elevated skin blood flow to dissipate heat.
Hyperthermia during pregnancy can cause embryonic death, abortion, growth retardation, and developmental defects; animal studies indicate that the
development of the CNS is especially susceptible.47
In humans, epidemiologic studies suggest that an
elevation of maternal body temperature by 2°C for at
least 24 hours during fever can cause a range of
developmental defects, although a causal relationship has not been established. In addition, young
infants aged 2 to 3 months are even more vulnerable
than neonates because of their higher metabolic rate,
better tissue insulation, and slightly lower surface
area/mass ratio. However, serious health effects are
associated only with greatly elevated body temperatures (⬎40°C), and such temperature rises are well
above the maximum allowable for public RF exposure.
Many different nonthermal mechanisms for RF interaction with tissue have been considered in recent
studies.48–50 These are not particular to children, but
if any were confirmed at levels below current guidance, then questions might also be raised about potential childhood susceptibility. Possible RF electricfield interactions51 include (1) changes in the
conformation of proteins, including ATPases associated with ion channels, resulting in functional
changes in the proteins, (2) changes in the binding of
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e309
ligands such as Ca2⫹ to cell receptor proteins, also
resulting in changed receptor function, (3) absorption of RF energy by the vibrational states of biological components such as microtubules, (4) enhanced
attraction between cells (the pearl-chain effect), and
(5) demodulation of a modulated RF signal, producing ELF electric fields. Generally, it was considered
that such interactions are unlikely to be biologically
significant at RF levels below guidance values.
In addition, there is evidence concerning RF interactions with magnetite affecting nearby ion channel
function by exerting a torque. Possible RF magnetic
field effects include (1) interaction with magnetite
particles in biological tissue and (2) radical pair
interactions, potentially increasing free-radical concentrations, thereby leading to an increased risk of
oxidative damage. Although these interaction mechanisms are also considered unlikely to be of biological significance at RF levels below guidance values,
given the link between free radicals and disease, RF
effects on free-radical concentrations via radical-pair
interactions are considered worth exploring.
For infant, childhood, and adolescent exposure,
the maturation of the CNS has been raised as potentially susceptible. In this context, the major changes
to the CNS during this period comprise a maturation
of the hard-wiring (namely, increased myelination),
facilitating the transmission of information, which
occurs rapidly over the first 2 years but extends into
the second decade of life, and remodeling of the
synaptic connections between neurons8 after the first
2 years and into adolescence, mostly by synapse
elimination as redundant connections are lost. With
regard to synaptogenesis, spontaneous and stimulus-evoked electrical activity in the CNS is believed
to play a crucial role in local competition between
growing nerve axons and the distribution of their
synaptic boutons on target cells.52 Whether RF fields
could affect these processes is not known. Neurobehavioral studies in volunteers and in animals, mostly
adults, have not reported robust responses to RF
exposure, particularly that associated with mobile
phones.31
Numerous studies have evaluated developmental
effects of RF fields on mammals, birds, and other
nonmammalian species.53,54 These studies have
shown clearly that RF fields are teratogenic at exposure levels that are high enough to cause significant
increases in temperature. There is no consistent evidence of effects at nonthermal exposure levels, although only a few studies have evaluated possible
effects on postnatal development using sensitive end
points such as behavioral effects.
Several studies of maternal occupational RF exposure, primarily to physiotherapists, have reported an
increased risk of congenital malformations. However, no specific type of malformation has been consistently reported, and there is a potential for recall
bias in these studies. Exposure to the fetus from a
mobile phone kept in a pocket, handbag, or belt by
the hip when a pregnant woman is using hands-free
equipment has been mentioned. Thus far, no studies
are available on pregnancy outcomes related to mobile telephony.
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All the studies have reported negative results for
carcinogenicity in normal animals at SARs compatible with mobile telephony,55 although controversy
still exists about the carcinogenic effects of RF radiation in a transgenic mouse model.56 Two studies in
particular reported the lack of an effect of perinatal
RF exposure, continuing for 24 months, on spontaneous and chemically induced brain tumors in
rats.57,58
Several ecological studies59–66 have examined cancer risk, including risk of childhood leukemia,
among populations living in proximity to radio and
television broadcast towers. Often driven by a previously identified cluster, these analyses are based
simply on distance from the source and often include
an extremely small number of cases. Such studies
have been uninformative. More rigorous investigations might be feasible with development of new
instruments capable of capturing personal RF exposure.
Few relevant epidemiologic or laboratory studies
have addressed the possible effects of RF exposure
on children. Because of widespread use of mobile
phones among children and adolescents and relatively high exposures to the brain, investigation of
the potential effects of RF fields on the development
of childhood brain tumors is warranted. The importance of longer lifetime exposure has been emphasized by a recent study67 in which acoustic neuroma
occurred only after 10-year use of mobile phones.
The type of mobile-phone use among children (eg,
text messaging), their potential biological vulnerability, and longer lifetime exposure make extrapolation
from adult studies problematic. Such scientific uncertainty can be addressed through both the application of precautionary policies and through additional
research.
DEVELOPING POLICY FOR CHILDREN AND
PREGNANT WOMEN
In today’s world, technologic developments bring
both social and economic benefits to large sections of
society; however, the health consequences of these
developments can be difficult to predict and manage.
Nevertheless, even if the effects are small, a widespread exposure can have large public health consequences. When risks are complex, an established
cause-effect relationship is absent, or the scientific
findings are not robustly quantifiable, the need for
timely preventive action makes a precautionary approach an essential part of policy making. Many
societies believe that this is particularly true regarding children (including the unborn child): they represent the future of the society, have the potential for
longer exposure than adults, and yet are less able to
manage their own risk.
International guidance on occupational and public
exposure to EMFs, described above, is based on
avoiding risks to health that are well understood and
for which there is good scientific evidence. However,
with regard to childhood exposure to EMFs (and
exposure during pregnancy), several factors argue
for the adoption of precautionary measures, including the possibility that EMFs might affect children;
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the dread with which some of the diseases raised in
this context, such as leukemia and brain cancer, are
perceived; the involuntary nature of some of the
exposure; its extensiveness; and its likely rapid
growth in the future.
The WHO International EMF Project (www.who.
int/emf) is finalizing a practical framework for guiding policy options in areas of scientific uncertainty
that is based on the application of precaution.68 In
general terms, the draft WHO precautionary framework aims to develop a set of public health policy
options that can be applied according to the degree
of scientific uncertainty and the anticipated severity
of the harm that might ensue from exposure, taking
into account the size of the affected population and
the cost of exposure reduction. These measures
should not be seen as undermining science-based
guidance on exposure; rather, they represent additional steps with application that may vary from
country to country depending on social and economic considerations.
Precautionary measures may also be adopted at an
individual level, depending on the degree of concern
felt by the exposed person. In giving advice to their
patients, physicians should weigh the strength of
scientific evidence for the risk, if any, of an adverse
outcome, the benefits of the technology, and the feasibility of reducing exposure, as well as the overall
health of the patient, which includes freedom from
worry and anxiety.
For ELF (power-frequency) fields, there is some
evidence that exposure to environmental magnetic
fields that are relatively high but well below guidance levels is associated with an increase in the risk
of childhood leukemia, a very rare disease (even if
the risk is doubled, it remains small at ⬃5– 8 per
100 000 children per year). Although the evidence is
regarded as insufficient to justify more restrictive
limits on exposure, the possibility that exposure to
ELF magnetic fields increases risk cannot be discounted. For the physician faced with questions
from, for example, a couple planning a family and
concerned about this issue, or from someone pregnant and occupationally exposed to relatively high
ELF magnetic fields, standardized advice is not possible. Instead, physicians could inform their patients
of possible risk and advise them to weigh all the
advantages and disadvantages of the options available to them (of which EMF reduction is but one
consideration). Some simple options include reducing exposure by minimizing the use of certain electrical appliances or changing work practices to increase distance from the source of exposure. People
living near overhead power lines should be advised
that such proximity is just an indicator of exposure
and that homes far away from power lines can have
similar or higher fields.
Regarding the long-term health effects of mobilephone use, the paucity of data, particularly for children, suggests that low-cost precautionary measures
are appropriate, especially because some of the exposures are close to guideline limits. Physicians
could advise parents that their children’s RF exposure can be reduced by restricting the length of calls
or by using hands-free devices to keep mobile
phones away from the head and body. On the other
hand, exposure levels from mobile-phone base stations are extremely low, and therefore precautionary
measures do not need to be recommended.
RESEARCH RECOMMENDATIONS
In addition to reviewing the available evidence
summarized in this article, workshop participants
developed a research agenda that identifies highpriority studies needed to fully assess the potential
vulnerability of children to ELF and RF fields and
outlines the rationale for these studies (see www.
who.int/peh-emf/research/rf03/en for more details). Additional laboratory and epidemiologic studies relating to childhood leukemia and ELF magnetic
field exposure were strongly recommended. In addition, because of widespread use of mobile phones
and relatively high exposures to the brain among
children and adolescents, investigation of the potential effects of RF fields on cognition and the development of childhood brain tumors was considered
particularly urgent. Laboratory studies using children are, of course, subject to appropriate ethical
design and approval.
APPENDIX: GLOSSARY
Absorption: dissipation of the energy of a radio wave
(ie, conversion of its energy into another form, such
as heat) into the surrounding medium.
Basic restriction: restriction on exposure to time-varying electric, magnetic, and electromagnetic fields that
are based directly on established health effects. Depending on the frequency of the field, the physical
quantities used to specify these restrictions are current density (J), SAR, and power density (S). Only
power density in air, outside the body, can be readily
measured in exposed individuals.
Contact current: current flowing through a person in
contact with 2 surfaces that are at different potentials.
Current density: a vector of which the integral over a
given surface is equal to the current flowing through
the surface; the mean density in a linear conductor is
equal to the current divided by the cross-sectional
area of the conductor; expressed in ampere per
square meter (A/m2).
Dosimetry: measurement or determination by calculation of the internal electric-field strength or induced current density, or of the specific absorption
(SA) or SAR distribution in humans or animals exposed to EMF.
Electric field or electric-field strength (E): the force (E)
on a stationary unit positive charge at a point in an
electric field; measured in volts per meter (V/m).
Electric and magnetic fields or electromagnetic fields
(EMFs): the combination of time-varying electric and
magnetic fields.
Extremely low frequency (ELF) EMFs: EMFs at frequencies of ⬎0 Hz and ⬍300 Hz.
Field strength: the magnitude of the electric or magnetic field, normally the root-mean-square value.
Frequency: the number of sinusoidal cycles completed
by electromagnetic waves in 1 second; usually expressed in units of hertz (Hz).
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Induced current: current induced in a human body
exposed to EMF.
Magnetic field or magnetic field strength (H): an axial
vector quantity, H, which, together with magnetic
induction, specifies a magnetic field at any point in
space; expressed in units of ampere per meter (A/
m2).
Magnetic flux density (B): a vector field quantity, B,
that results in a force that acts on a moving charge or
charges; expressed in tesla (T) or gauss (G).
Nonionizing radiation: includes all radiation and fields
of the electromagnetic spectrum that do not normally
have sufficient energy to produce ionization in matter; characterized by energy per photon less than
⬃12 eV, wavelengths ⬎100 nm, and frequencies ⬍3
⫻ 1014 Hz.
Power density: the rate of electromagnetic energy flow
crossing a unit area normal to the direction of wave
propagation; expressed in watts per square meter
(W · m⫺2).
Power frequency: the frequency at which alternatingcurrent electricity is generated. For electric utilities,
the power frequency is 60 Hz in North America,
Brazil, and parts of Japan. Electric power is 50 Hz in
much of the rest of the world. Isolated alternatingcurrent electrical systems may have other power frequencies, eg, 440 Hz in commercial airliners and 162⁄3
Hz in some railway systems.
Radiation (electromagnetic): the emission or transfer of
energy through space in the form of electromagnetic
waves.
Radio frequency (RF): any frequency at which electromagnetic radiation is useful for telecommunication.
In this article, RF refers to the frequency range of 10
MHz to 300 GHz.
Reference level: EMF exposure level provided for practical exposure-assessment purposes to determine if
basic restrictions are likely to be exceeded. Some
reference levels are derived from relevant basic restrictions using measurement and/or computational
techniques, and some address perception and adverse indirect effects of exposure to EMF.
Specific absorption: the energy absorbed per unit mass
of biological tissue, expressed in joules per kilogram
(J/kg); specific absorption is the time integral of the
SAR.
Specific absorption rate (SAR): the rate at which energy
is absorbed in body tissues; expressed in watts per
kilogram (W/kg); SAR is the dosimetric measure
that has been widely adopted at frequencies above
⬃100 kHz.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
ACKNOWLEDGMENTS
The workshop was funded by the World Health Organization,
Electric Power Research Institute, the European programs EMFNET and COST281, and Statens Strålskyddsinstitut of Sweden.
We are grateful to all participants of the expert group (see
www.who.int/peh-emf/research/rf03/en for a list of invited experts); Gail Lundell for scientific editing; and Sarah Bullock and
Riti Shimkhada for all organizational aspects.
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www.pediatrics.org/cgi/doi/10.1542/peds.2004-2541
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e313
The Sensitivity of Children to Electromagnetic Fields
Leeka Kheifets, Michael Repacholi, Rick Saunders and Emilie van Deventer
Pediatrics 2005;116;303-313
DOI: 10.1542/peds.2004-2541
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